Tree Physiology Advance Access published January 9, 2015

Tree Physiology 00, 1–7

doi:10.1093/treephys/tpu108

Letter

Downloaded from http://treephys.oxfordjournals.org/ at Universitaet Erlangen-Nuernberg, Wirtschafts- und Sozialwissenschaftliche Z on January 13, 2015
Distilling allometric and environmental information from
time series of conduit size: the standardization issue and
its relationship to tree hydraulic architecture
Marco Carrer1,3, Georg von Arx2, Daniele Castagneri1 and Giai Petit1

1Università
degli Studi di Padova—Dip. TeSAF, Agripolis, I-35020 Legnaro (PD), Padova, Italy; 2Swiss Federal Institute for Forest, Snow and Landscape Research WSL,
Birmensdorf, Switzerland; 3Corresponding author (marco.carrer@unipd.it)

Received August 5, 2014; accepted November 13, 2014; handling Editor Danielle Way

Trees are among the best natural archives of past environmental information. Xylem anatomy preserves information related
to tree allometry and ecophysiological performance, which is not available from the more customary ring-width or wood-­
density proxy parameters. Recent technological advances make tree-ring anatomy very attractive because time frames of
many centuries can now be covered. This calls for the proper treatment of time series of xylem anatomical attributes. In this
article, we synthesize current knowledge on the biophysical and physiological mechanisms influencing the short- to long-term
variation in the most widely used wood-anatomical feature, namely conduit size. We also clarify the strong mechanistic link
between conduit-lumen size, tree hydraulic architecture and height growth. Among the key consequences of these biophysi-
cal constraints is the pervasive, increasing trend of conduit size during ontogeny. Such knowledge is required to process time
series of anatomical parameters correctly in order to obtain the information of interest. An appropriate standardization pro-
cedure is fundamental when analysing long tree-ring-related chronologies. When dealing with wood-anatomical parameters,
this is even more critical. Only an interdisciplinary approach involving ecophysiology, wood anatomy and dendrochronology
will help to distill the valuable information about tree height growth and past environmental variability correctly.

Keywords: cell chronology, dendrochronology, signal versus noise, tree-ring anatomy, wood anatomy, xylem hydraulic
response.

Introduction
Trees are impressive life forms. Being sessile and long-living
organisms that occur across a vast range of contrasting environ-
ments and under a variety of disturbance regimes, they must be
able to cope with many different internal and external changes
(Hinckley et al. 2011). During ontogenetic development, the
size of a tree increases by many orders of magnitude, which is
paralleled by a constant adjustment of tree structure to main-
tain the capacity to procure and transport resources from the
environment and to grow and reproduce despite the variability
of biotic and abiotic factors. Nevertheless, all trees develop with
the same basic anatomical and physiological design (Enquist
2003). In regions where detectable and reliable annual rings
are formed, the fluctuations of environmental conditions may
leave a permanent imprint on several measurable ring proper-
ties usually related to its width, structure and chemical compo-
sition (Hughes 2011). This coexistence of multiple properties
potentially contains distinct and complementary information
associated with biomass accumulation and environmental vari-
ability and explains why tree rings are among the most wide-
spread, precise and accurate natural archives (Bradley 1999,
Swetnam et al. 1999).
Among the different tree-ring properties, wood-anatomical
features represent an emerging set of parameters (Fonti et al.
2010). Conduit dimension, commonly expressed as cross-­
sectional lumen diameter or area, retains a special significance

© The Author 2015. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com
 2  Carrer et al.
within the anatomical tree-ring features because of its direct
link to the tree hydraulic architecture. Thanks to this, lumen
area could bridge some gaps between radial and axial growth
patterns and other tree responses related to environmental
variability, allometric constraints during ontogenesis and physi-
ological regulation. The increasing number of papers published
in recent years (for a thorough review, see Fonti et al. 2010)
confirms the promising potential of this approach (Drew et al.
2013, Fonti et al. 2013, Liang et al. 2013). However, a main
obstacle to the interpretation of the different types of informa-
tion in conduit-lumen patterns is the insufficient understanding
of the role of changing conduit dimension during ontogeny. This
is especially true because trees are mostly unselective and, in a
way, biased recorders. They are unselective in that many envi-
ronmental inputs that affect tree growth can leave an identical
signature within the tree-ring sequences and biased because,
being living organisms, this tracing is never a pure physical
process but is filtered and modulated by individual physiologi-
cal responses (Carrer 2011, Meinzer et al. 2011). Working with
tree-ring features such as conduit dimension therefore means
having to deal with this ambiguity between internal and external
(specific and unspecific) signals (Cook 1990).
Classical tree-ring research follows specific sampling criteria
designed to identify sites, species and trees (Fritts 1976, Cook
and Kairiukstis 1990), followed by a specific processing of the
ring-width series called standardization (Cook et al. 1990).
Standardization is of such outstanding importance in tree-ring
research that Fritts (1976) defined it as ‘such a basic procedure
in dendrochronology that it is considered by some to be a prin-
ciple’. The intent of standardization is manifold: (i) to remove
non-stationary processes related to the mostly size-related
(and to a lesser extent age-related) trend or disturbance pulses
(in the case of ring width, the generally decreasing trend with
age is due substantially to the geometric constraint of adding
an annual wood layer over an expanding surface represented
by the stem cross-section); (ii) to stabilize the variance of tree-
ring series, which are commonly heteroscedastic; and (iii) to
homogenize the growth rate among samples (despite living in
the same location, some trees grow faster and others slower;
therefore, it is better to assign the same weight to all samples
before they enter the mean growth curve; Cook et al. 1990,
Helama et al. 2004, Biondi and Qeadan 2008). Throughout
more than one century of tree-ring research, an endless num-
ber of different standardization methods have been proposed,
and the discussion about the optimal procedure is still very
active within the broad dendrochronological community (Melvin
and Briffa 2008, Nicault et al. 2010, Briffa and Melvin 2011).
In time series of wood-anatomical ring properties, such
as conduit-lumen area, defining the appropriate standardiza-
tion approach for the specific information of interest is par-
ticularly critical because knowledge from several research
fields, including tree physiology, dendrochronology and wood
Tree Physiology Volume 00, 2015
anatomy, is required. In the following, focusing on time series
of conduit-lumen area, we first give some relevant background
about long-term trends that usually govern this parameter. We
detail different aspects of how to extract environmental and
ontogenetic information from these data by using an appro-
priate standardization technique and illustrate this with exam-
ples. To conclude, we offer some guidelines and perspectives
for potential applications of the different kinds of information
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recorded in time series of conduit-lumen area.
The hydraulic constraints on conduit size
during ontogenesis
One of the main functions of xylem tissue is the delivery of
water throughout the plant from the rootlets up to the stomata
(Zimmerman 1983). To sustain optimal tree functioning, the
hydraulic system must be efficient and plastic in order to cope
with internal and external (i.e., environmental) variability. The
major source of internal variability is tree growth itself; during
ontogenesis, there is usually a significant increase in the path
length that water must cover. According to the classic Hagen–
Poiseuille formula, resistance through an ideal tube scales with
the fourth power of its diameter and linearly with length (Tyree
and Ewers 1991, West et al. 1999); therefore, if all xylem con-
duits were of the same diameter from the apex to the base,
the hydrodynamic resistance would increase linearly as the
tree grows in height. This could lead to catastrophic conse-
quences for plant physiology, either inducing water deficits due
to insufficient supply (Ryan and Yoder 1997) or necessitat-
ing osmotic adjustments to lower the leaf water potential and
sustain transpiration and leaf hydration under increasingly high
xylem tensions. This would trigger the risk of hydraulic failure
by cavitation, a primary cause of productivity loss and plant
mortality (Choat et al. 2012). However, by widening the diame-
ter of xylem conduits from the stem apex downwards, trees are
able to minimize the adverse effect of height growth on path-
way length resistance. In other words, downwards widening of
xylem conduits provides an effective mechanism to supply the
distal leaves with water irrespective of the absolute root-to-leaf
distance (Becker et al. 2000, Enquist 2002).
In recent years, a number of investigations have reported sub-
stantial conduit widening for vascular plants independent from
any species and organism size. The theoretical degree of widen-
ing towards which all plants should ‘universally’ converge is still
debated (see West et al. 1999, Savage et al. 2010), yet empiri-
cal data available in the literature, reporting the pattern of axial
variation of xylem conduit dimension against the distance from
the stem apex, suggest a convergence towards a power trajec-
tory (y = aLb, with y being the conduit dimension, a the allometric
constant and L the distance from the stem apex) with a scaling
exponent (b) varying slightly around 0.2 (Sperry et al. 2012, von
Allmen et al. 2012, Anfodillo et al. 2013, Olson and Rosell 2013,

Olson et al. 2014) throughout ontogeny (Weitz et al. 2006).
However, slight deviations from this general trend can be found
in the presence of significant mechanical constraints, where con-
duits are usually narrower (e.g., around the root collar or branch
junctions; Zimmerman 1983, Tyree and Alexander 1993), or
in tall trees, where xylem conduits seldom increase in size for
the first few metres from the ground (Mencuccini et al. 2007).
Nonetheless, these local deviations do not confute the overall
validity of the trees' general strategy of conduit widening.
The physiological mechanism behind this distinct pattern of
axial widening of xylem conduits still has to be identified pre-
cisely. However, hormonal signalling related to auxin produc-
tion and transport and the duration of cell expansion during
xylogenesis seem to play a key role in controlling the xyloge-
netic process (Aloni 2013) and the final conduit size (Anfodillo
et al. 2012), respectively.
The fact that the change in conduit dimension with cam-
bial age (i.e., from the pith outwards) reflects the adjustment
of the pathway length resistance to height growth (Anfodillo
et al. 2006) implies that it is not ageing per se (Petit et al.
2008) but rather the increase in tree height with ontogeny
that is the underlying driver of this pattern. In other words, the
conduit-lumen diameter in a tree increases with cambial age at
rates dependent on the rates of stem elongation. For instance,
assuming the hypothetical case of a constant annual height
Figure 1.  The typical theoretical age-related trend in tree height and the corresponding change in conduit dimension represented in the two upper
plots for three trees with different growth rates. This correspondence can be detected by following the conduit dimension either along the stem
within the same annual ring or across a section from the pith outwards.
Distilling information from time series of conduit size 3
growth from seedling to maturity, conduit diameter would like-
wise increase with cambial age according to a pattern very
similar to that of the axial widening (Figure 1).
Ideally, trees approach their maximal height soon after matu-
rity (Husch et al. 2003), and the imprint of this achievement on
anatomical characteristics can be identified in the levelling off
of the time series of conduit-lumen area (Anfodillo et al. 2006),
also known as Sanio's first law (Sanio 1872). This trend, visible
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in most of the cell chronologies after the cambial age of around
100 years and clearly evident in the longest ones (Figures 2
and 3), does not represent the only signal retained in the con-
duit-dimension series, yet it represents one of the most signifi-
cant and unambiguous ones (Figure 1). Thus, identification of
environmental signatures requires, as for tree-ring width series,
a disentanglement from such a long-term growth pattern.
Pervasive features in time series of conduit
dimension: dealing with standardization
Until now, most investigations on conduit dimension have
focused on short- (few years; Rossi et al. 2008, Gricar et al.
2011) to medium-term (few decades) time scales (Fonti et al.
2007, Olano et al. 2012). In these cases, standardization is
not that critical, either because the time period considered
is too short or because most of the researchers adopted the
Tree Physiology Online at http://www.treephys.oxfordjournals.org
 4  Carrer et al.

classical dendrochronological approach of sampling the old-

est and biggest trees, thus avoiding the early years/decades
with the common significant increase in conduit dimension.
However, the recent progress in digital image-analysis systems
now allows series of wood-anatomical features to be extended
to time scales similar to those of other tree-ring parameters
(von Arx and Carrer 2014). Consequently, to make proper use
of the potential, three pervasive features should be considered

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when building conduit-size chronologies in order to improve
the extraction of the signal of interest and the selection of the
most appropriate method to standardize the series:

Figure 2. Time series of conduit-lumen area extracted from a Picea
abies sample (PIAB3 in Table S2 available as Supplementary Data
at Tree Physiology Online) using different percentiles and the aver-
age size of the three widest conduits (MAX3). The monotonic power-
related increasing trend is always visible except when considering the
fifth percentile. See Figure 3 caption and Tables S1 and S2 available as
Supplementary Data at Tree Physiology Online for further information
on the sample, data collection and regression statistics.
(i) The increasing trend. The typical monotonic increasing trend
of conduit size becomes apparent from Figures 1 and 2.
This trend is appreciable whichever statistics we choose to
express the yearly value of conduit dimension. It only disap-
pears when choosing the fifth percentile, i.e., selecting only
the smallest conduits per year. Indeed, the minimal conduit

Figure 3.  Comparison of time series of ring width and 90th percentile conduit-lumen area among different species. For an easier comparison, raw
series (left panels) have been rescaled, dividing each yearly value by the corresponding mean series value. Note the high variability in the tree-ring
sequences compared with the convergence in the long-term pattern of conduit area. The right axis for the raw series of conduit area refers to the
Quercus sp. and Fagus samples. Samples are from different species (P. abies, Larix decidua, Pinus sylvestris, Pinus leucodermis, Juniperus thurifera,
Betula pubescens, Fagus sylvatica and Quercus sp.) and different regions (high and low elevation in the Alps and Siberia), with different wood
anatomy (ring-porous, diffuse-porous and coniferous), evergreen vs deciduous and grown in different historic times (relic oak sample vs dead
or living trees). We selected one core per species, paying attention to include or be very close to the pith in order to catch most of the early-life
dimensional change in conduit-lumen area. We were consistent in processing, measuring and analysing the material; all samples were prepared
following the standard protocol for wood microscopical analysis (Fonti and Garcia-Gonzalez 2008, Gärtner and Schweingruber 2013), and digital
images were automatically processed and analysed using the image analysis tool ROXAS v1.6 (Fonti et al. 2009, Wegner et al. 2013, von Arx and
Carrer 2014). We measured almost all the conduits visible in each image with only minor editing. The number of conduits per ring was 12–25,285,
with an average value (mean ± SD) of 149 ± 338 for the angiosperms and 2087 ± 2242 for the conifers. More information on the samples can be
found in Table S2 available as Supplementary Data at Tree Physiology Online.

Tree Physiology Volume 00, 2015


size can be considered a threshold value rather stable in
time and defined by both biophysical and methodological
limits; a xylem conduit cannot be indefinitely small, and our
capacity to detect small conduits is bound to sample prepa-
ration, magnification, image resolution and other technical
issues. On the contrary, the increasing trend is stronger for
the largest conduits. This is because they contribute the
most to overall water transport and thus are under the stron-
gest control to maintain constant the pathway length resis-
tance as the tree grows taller.
(ii) The consistency of the trend. Figure 3 depicts the paral-
lel measurements of ring width and conduit lumen from
the same cores. Despite all the differences among sam-
ples, the overall long-term trend in conduit size is very
similar and significantly more consistent than that of ring
width (Figure S1 available as Supplementary Data at Tree
Physiology Online). It simply represents the yearly imprint
of height growth on the anatomical features of the xylem.
Dendrochronological and tree-ring anatomical investiga-
tions should consider this trend as the common major
component of long-term variability in conduit dimension.
Unless the research topic focuses on height growth, this
trend represents a component similar to the one related
to stem diameter and ring width and should often be
removed, or at least considered, to reveal the other infor-
mation retained in the tree-ring series (Cook 1990).
(iii) The smaller decadal variability in conduit size compared
with ring width. Abrupt growth changes in tree-ring width
sequences, i.e., transient pulses of growth releases or
suppressions, are a common feature in most samples
coming from the interior of closed-canopy forests or
from sites ­ previously affected by any forest disturbance
(Schweingruber et al. 1986). Conduit-lumen area is less
prone to these abrupt changes (Figure 3, Figure S1 ­available
as Supplementary Data at Tree Physiology Online). A tree can
significantly change its stem-diameter growth rate and may
even stop growing for a few consecutive years, but it always
has to ensure the delivery of water to the top of the crown,
because it is very unlikely that it could undergo dramatic
changes in its height and therefore in its conduit dimension.
As in tree-ring research, there is probably no single strict rule to
adopt for the standardization of conduit-dimension chronologies
because this depends on the specific scientific question under
investigation. However, any valid standardization approach
should be in agreement with the hydraulic constraints on con-
duit size during ontogenesis and the aforementioned related
pervasive features. Stochastic methods (e.g., smoothing spline,
Gaussian filters) are very flexible and may therefore always
be appropriate as long as they are tuned to keep the infor-
mation of interest in relationship to the characteristics of the
series. Among the deterministic methods, power functions are
Distilling information from time series of conduit size 5
particularly appropriate because they have a sound biophysical
basis (i.e., related to the axial widening of xylem conduits and
average stem elongation during ontogeny), whereas the nega-
tive exponential models used for ring-width series are clearly
inappropriate. Lastly, methods such as the regional curve stan-
dardization (Briffa and Melvin 2011) should perform like the
power functions in view of the consistent height-related trend.
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Outlook on some practical applications
Time series of lumen size (cross-sectional diameter or area) of
xylem conduits encode information about the relationship with
tree height development, which does not necessarily correspond
to ring-width growth patterns. The universal and consistent
increasing trend of time series of conduit size until tree matu-
rity, typically expressed by a power function, implies that any
deviation will reflect positive or negative pulses of height growth.
Adequate consideration of this fact allows time series of lumen
size to be used optimally for some interesting applications.
First, on a sub-annual basis, while photoperiod seems to
control the rate of cell production (Rossi et al. 2006) and the
final conduit size undergoes a form of apical control owing to
the duration of enlargement (Anfodillo et al. 2012), the over-
all process of conduit formation lasts not much longer than a
couple of weeks for the earlywood tracheids of a mature coni-
fer (Rossi et al. 2013). This fact, when combined with the pre-
cise position of each conduit within the ring, potentially allows
a phenological-based tuning of the time windows for the cli-
mate–growth association up to the sub-monthly or fortnightly
level. This would permit, for example, the extraction of detailed
climate information not only related to the mean monthly or
seasonal modes but also on the role of extreme events (e.g.,
heatwaves, mechanical damage related to wind storms, frost
events during the growing season) that often occur on much
shorter time scales but can leave profound legacies (e.g., wind
damage, reduction of living biomass, loss of branches) at the
ecosystem level (Babst et al. 2012).
Second, on an annual basis, adding an anatomical measure,
such as conduit size, can help to improve handling of the well-
known age-related issues that frequently afflict the information
extracted with the classical set of tree-ring parameters (Briffa
and Melvin 2011). More specifically, tree-ring-based climate
reconstructions might benefit from the introduction of conduit-
size chronologies; the latter quantify the ‘void’ in the wood,
which is therefore somehow the opposite of the well-established
density measurements. Nevertheless, the biologically related
trends in conduit size are fully independent of those of the
other tree-ring parameters. Comparing time–frequency domains
among different parameters could thus help in distinguishing the
climatic signature from the other components.
Finally, on a multi-annual level, conduit-size chronologies,
together with ring width, density and basal-area increment,
Tree Physiology Online at http://www.treephys.oxfordjournals.org
 6  Carrer et al.
could allow a much more accurate estimate of the wood pro-
duction and of long-term changes in carbon sequestration.
Recent studies proved that it is possible to combine biomet-
ric and eddy-covariance quantifications of carbon allocation
to different storage pools with classical tree-ring parameters
(Babst et al. 2014). This new link with conduit size adds a bet-
ter estimation of height growth and will probably contribute to
a better quantification of terrestrial carbon uptake, reducing
the uncertainties linked to the carbon cycle–climate feedback
mechanisms (Pan et al. 2011). The intriguing perspective is
that, focusing on the most likely power-function-related axial
pattern of conduit dimensions from trees of various age and
epochs, it will be possible to make a quantitative comparison of
present and past tree height growth. Parameterization of future
vegetation models could be greatly improved by introducing
long-term dynamic information related to height development
(Keith et al. 2010, McMahon et al. 2010, Meinzer et al. 2011,
Stephenson et al. 2014).
Concluding remarks
The recent technological advances in image analysis applied
to the field of wood anatomy open up a fascinating perspec-
tive for dendroecological studies that cover time frames as long
as the more established ring-width or wood-density chronolo-
gies. This creates the need to achieve a better understanding
of the biophysical and physiological mechanisms influencing
the short- to long-term variation in wood-anatomical features.
Only then will a sound standardization of long time series be
possible, and only then can the maximal potential of tree-ring
anatomy be exploited fully. In this article, we provide such a
background to one of the most promising anatomical features,
conduit-lumen area. Knowledge of the mechanistic relation-
ships between lumen dimension, tree hydraulic architecture and
height growth will permit the information recorded at the ana-
tomical level to be extracted. Applying an appropriate standard-
ization technique and being able to understand the long-term
trends in conduit-lumen area will probably allow long chronolo-
gies to be related to intra-annual climate fluctuations, as well as
the extraction of valuable information about tree height growth.
Supplementary data
Supplementary data for this article are available at Tree
Physiology Online.
Acknowledgments
The authors thank M. Bryukhanova, N. Bleicher, J. Camarero,
J. Esper, D. Martin-Benito, E. Pellizzari, A. Pacheco Solana and
A. Stritih for providing part of the material and some of the
measurements.
Tree Physiology Volume 00, 2015
Conflict of interest
None declared.
Funding
G.v.A. was supported by the Swiss State Secretariat for
Education, Research and Innovation, SERI (SBFI C12.0100). D.C.
Downloaded from http://treephys.oxfordjournals.org/ at Universitaet Erlangen-Nuernberg, Wirtschafts- und Sozialwissenschaftliche Z on January 13, 2015
was supported by the University of Padua (Research Project
D320.PRGR13001, Senior Research Grants 2012). This work
and the authors have been supported by the COST Action
STReESS (FP 1106).
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